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The Prevalence and Clinical Significance of Anaerobic Bacteria antibiotics Article The Prevalence and Clinical Significance of Anaerobic Bacteria in Major Liver Resection Jens Strohäker *, Sophia Bareiß, Silvio Nadalin, Alfred Königsrainer , Ruth Ladurner and Anke Meier Department of General, Visceral and Transplantation Surgery, University Hospital of Tuebingen, 72076 Tuebingen, Germany; [email protected] (S.B.); [email protected] (S.N.); [email protected] (A.K.); [email protected] (R.L.); [email protected] (A.M.) * Correspondence: [email protected]; Tel.: +49-7071-29-68171 Abstract: (1) Background: Anaerobic infections in hepatobiliary surgery have rarely been addressed. Whereas infectious complications during the perioperative phase of liver resections are common, there are very limited data on the prevalence and clinical role of anaerobes in this context. Given the risk of contaminated bile in liver resections, the goal of our study was to investigate the prevalence and outcome of anaerobic infections in major hepatectomies. (2) Methods: We retrospectively analyzed the charts of 245 consecutive major hepatectomies that were performed at the department of General, Visceral, and Transplantation Surgery of the University Hospital of Tuebingen between July 2017 and August 2020. All microbiological cultures were screened for the prevalence of anaerobic bacteria and the patients’ clinical characteristics and outcomes were evaluated. (3) Results: Of the 245 patients, 13 patients suffered from anaerobic infections. Seven had positive cultures from the biliary tract during the primary procedure, while six had positive culture results from samples obtained during the management of complications. Risk factors for anaerobic infections were preoperative biliary stenting (p = 0.002) and bile leaks (p = 0.009). All of these infections had to be treated by Citation: Strohäker, J.; Bareiß, S.; intervention and adjunct antibiotic treatment with broad spectrum antibiotics. (4) Conclusions: Nadalin, S.; Königsrainer, A.; Ladurner, Anaerobic infections are rare in liver resections. Certain risk factors trigger the antibiotic coverage R.; Meier, A. The Prevalence and of anaerobes. Clinical Significance of Anaerobic Bacteria in Major Liver Resection. Keywords: anaerobic infection; liver resection; cholangitis; biliary tract infection Antibiotics 2021, 10, 139. https:// doi.org/10.3390/antibiotics10020139 Academic Editor: Fernando Cobo 1. Introduction Received: 6 January 2021 Accepted: 28 January 2021 Liver resections are widely available procedures to cure benign and malignant diseases Published: 31 January 2021 of the liver. After partial hepatectomy bile leaks and surgical site infections, complications are feared, since they drastically increase morbidity and mortality [1–3]. Liver resections Publisher’s Note: MDPI stays neutral are considered clean-contaminated procedures given the risk of preexisting bacterial and with regard to jurisdictional claims in fungal colonization of the biliary system. The most common bacteria cultured from the bile published maps and institutional affil- duct and postoperative infectious complications are of gastrointestinal origin [4–6]. iations. Anaerobic liver infections, however, are rare in hepatobiliary surgery. The most com- monly described presentation of anaerobes in the liver is in the form of liver abscesses. These abscesses are frequently caused by acute or chronic abdominal inflammation or infection [7,8]. Recently, an emerging number of abscesses have been of iatrogenic origin, Copyright: © 2021 by the authors. caused by percutaneous ablation of primary and secondary liver malignancies. Abscesses Licensee MDPI, Basel, Switzerland. after ablation appear to develop in up to 2% of patients [9,10]. Anaerobic bacteria are com- This article is an open access article mon pathogens in the intestines. The liver and native biliary tract are generally uncommon distributed under the terms and habitats for anaerobic bacteria. However, they may be cultured from the biliary tract in up conditions of the Creative Commons to 20% of patients in the presence of a biliary tract occlusion or stent [11,12]. Aside from Attribution (CC BY) license (https:// biliary stents, bilioenteric anastomoses are considered a risk factor for anaerobic coloniza- creativecommons.org/licenses/by/ tion and infection of the biliary tree (and liver). Therefore, the 2018 Tokyo Guidelines 4.0/). Antibiotics 2021, 10, 139. https://doi.org/10.3390/antibiotics10020139 https://www.mdpi.com/journal/antibiotics Antibiotics 2021, 10, 139 2 of 12 (TG2018) recommend covering anaerobic bacteria when treating cholangitis in the presence of bilioenteric anastomosis [13]. The department of General, Visceral, and Transplantation Surgery of the Tuebingen University Hospital is a Tertiary Care Academic Teaching facility that performs an av- erage of ~200 liver resections as well as ~50 liver transplantations per year. Our center is specialized on complex liver resections with a clinical and scientific focus on biliary malignancies. [14,15]. A major hepatectomy/liver resection is defined as the removal of ≥3 liver segments [16]. Due to biliary obstruction of perihilar malignancies, patients often present with jaundice or have undergone preoperative stenting and are thus at risk of biliary tract infections [12]. Infectious complications after surgery are still a major risk factor for morbidity and mortality after liver resection. Surgical site and organ-space infections present in up to 20% of major hepatectomies [1,17]. The role of anaerobic bacteria is yet to be assessed. To our knowledge, there are neither sufficient data on the presence of anaerobes in intraoperative microbiological specimen from liver resections nor from surgical site infection (SSI) after hepatectomy. Even less is known about the presence of anaerobic bacteria’s antibiotic resistance to commonly used antibiotics after liver surgery. The goal of this study was to evaluate the prevalence and clinical role of anaerobic bacteria in patients undergoing major liver resection for benign and malignant disease. 2. Results 2.1. Clinical Characteristics We analyzed the charts of all consecutive patients that had undergone major liver resec- tion at the department of General, Visceral, and Transplantation Surgery of the Tuebingen University Hospital from June 2017 to August 2020. We included all adult (age ≥ 16 years) consecutive patients that underwent laparotomy and had at least three liver segments removed. Pediatric patients, as well as patients that had minor liver resections, were ex- cluded. Based on the preoperative diagnosis and intraoperative findings, material was sent for microbiological testing at the attending surgeon’s discretion. During the study period, 245 patients met the inclusion criteria. Of these 245 patients, 76 had intraoperative material sent for microbiological testing, of which 49 showed growth of pathogenic bacteria. Furthermore, 102 of the 245 patients had culture-proven microbio- logical growth during the first 30 postoperative days (this includes the 49 that had growth on the intraoperative cultures). From these 102 patients, we were able to identify 13 pa- tients that had anaerobic infections. Of these 13 patients, 7 patients had positive anaerobic cultures from specimens that were collected during under the primary surgical procedure. The remaining six patients had positive anaerobic cultures during revision (n = 5) pro- cedures or from specimen collected from drains (n = 1). The median age was 60 years (Standard Deviation (SD) ±15, range 34–80). Five patients were male (38%), and eight were female (62%). Most patients underwent liver resection for malignancy (n = 9), while the other patients were treated for helminthic disease (n = 2), suspected cholangiocarcinoma (n = 1), and recurrent cholangitis after cholecystectomy (n = 1). Of the 13 patients, 9 patients received prolonged perioperative antibiotics for suspected contaminated biliary tract (n = 3) or risk of post-hepatectomy liver failure (PHLF) (n = 6). These patients had anaerobic coverage with metronidazole (n = 6) or piperacillin/tazobactam (n = 2) or meropenem (n = 1). For details, see Table1. Antibiotics 2021, 10, 139 3 of 12 Table 1. The surgical procedures and outcomes, as well as the isolated anaerobic strains of the 13 patients that had positive anaerobic cultures. * Procedures according to Brisbane classification. Surgical Details and Outcome Location of Preoperative Age, Gender Diagnosis Procedure Anaerobe Complications Length of Stay Outcome Specimen Stent Right Trisectionectomy * Prevotella buccae + Resection of Bile duct 34 f iCCA Prevotella Yes 11d alive Extrahepatic bile duct and 1st Procedure melaninogenica bilioenteric anastomosis Right Trisectionectomy death from septic Anaerobe not + Resection of Bile duct shock due to 72 m HCC otherwise Yes 29d dead Extrahepatic bile duct and 1st Procedure post-hepatectomy specified bilioenteric anastomosis liver failure death from multi-organ failure with bile Embryonal Right Trisectionectomy Anastomotic leak Bacteroides leak and 44 w Sarcoma of the No 35d dead + Segmental Colectomy Revision vulgatus peritonitis Liver & post-hepatectomy liver failure Right Trisectionectomy Echinococcus + Resection of Bile duct Bifidobacterium 38 m Yes 28d alive alveolaris Extrahepatic bile duct and 1st Procedure animalis bilioenteric anastomosis Left Hepatectomy + Resection of Bile duct Bacteroides 71 m phCCA Yes 13d alive Extrahepatic
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